Skip to main content
Log in

The disruption of habitat isolation among three Hexagrammos species by artificial habitat alterations that create mosaic-habitat

  • Original Article
  • Published:
Ecological Research

Abstract

In the coastal areas of Japan, three species of greenling (Hexagrammos spp.) can hybridize. In a natural reef setting we showed that Hexagrammos agrammus and H. octogrammus established their breeding territories in a shallow area where seaweed was abundant, whereas H. otakii established breeding territories in a deep area that was sparsely covered with seaweed. This difference in habitat use resulted in H. otakii being distributed separately from the other two species, thereby reducing the potential for hybridization. However, all the three species co-occurred in an artificial area near a breakwater. This area is characterized by steep slopes and complex stacked concrete structures, which create a mosaic-habitat consisting of a shallow environment with seaweed and a deep environment with sparse seaweed, allowing the three species to breed within a single area. Our results suggest that man-made structures can create an artificial mosaic-habitat that can disrupt habitat isolation and promote hybridization between species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Amaoka K (1984) Family Hexagrammidae. In: Masuda H, Amaoka K, Araga C, Urno T, Yoshino T (eds) The fishes of the Japanese Archipelago (in Japanese). Tokai University Press, Tokyo, pp 320–321

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Balanov AA, Markevich AI, Antonenko DV, Crow KD (2001) The first occurrence of hybrids of Hexagrammos otakii × H. octogrammus and description of H. otakii from Peter the Great Bay (The Sea of Japan). J Ichthyol 41:728–738

    Google Scholar 

  • Bierne N, Bonhomme F, David P (2003) Habitat preference and the marine-speciation paradox. Proc R Soc Lond B Biol Sci 270:1399–1406

    Article  Google Scholar 

  • Bridle JR, Baird SJE, Butlin RK (2001) Spatial structure and habitat variation in a grasshopper hybrid zone. Evolution 55:1832–1843

    CAS  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates Inc, Massachusetts

    Google Scholar 

  • Crow KD, Powers DA, Bernardi G (1997) Evidence for multiple maternal contributors in nests of kelp greenling (Hexagrammos decagrammus, Hexagrammidae). Copeia 1997:9–15

    Article  Google Scholar 

  • Crow KD, Munehara H, Kanamoto Z, Balanov A, Antonenko D, Bernardi G (2007) Maintenance of species boundaries despite rampant hybridization between three species of reef fishes (Hexagrammidae): implications for the role of selection. Biol J Linn Soc Lond 91:135–147

    Article  Google Scholar 

  • Eisenhour DJ, Piller KR (1997) Two new intergeneric hybrids involving Semotilus atromaculatus and the genus Phoxinus with analysis of additional Semotilus atromaculatusPhoxinus hybrids. Copeia 1997:204–209

    Article  Google Scholar 

  • Estrada C, Jiggins CD (2002) Patterns of pollen feeding and habitat preference among Heliconius species. Ecol Entomol 27:448–456

    Article  Google Scholar 

  • Gorbunova NN (1970) Spawning and development of greenlings (Family Hexagrammidae). In: Rass TS (ed) Greenlings: taxonomy, biology and interoceanic transplantation. Israel Program for Scientific Translations, Moskva, pp 121–185

    Google Scholar 

  • Kanamoto Z (1976a) On the ecology of Hexagrammid fish. 1) Habitats and behaviors of Agrammus agrammus (Temminck et Schlegel) and Hexagrammos otakii (Jordan et Starks) (in Japanese with English abstract). Jpn J Ecol 26:1–12

    Google Scholar 

  • Kanamoto Z (1976b) On the ecology of Hexagrammid fish. 2) The distribution of Hexagrammid fish (in Japanese). Nihon suisan gakkai tohoku sibu kaiho 26:48–53

    Google Scholar 

  • Lamb T, Avise JC (1986) Directional introgression of mitochondrial DNA in a hybrid population of tree frogs: the influence of mating behavior. Proc Natl Acad Sci USA 8:2526–2530

    Article  Google Scholar 

  • Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Munehara H (2001) Mating and paternal care behavior of Hexagrammid fishes. In: Amaoka K (ed) The story of fishes––biodiversity of fishes (in Japanese). Tokai University Press, Tokyo, pp 151–167

    Google Scholar 

  • Munehara H, Kanamoto Z, Miura T (2000) Spawning behavior and interspecific breeding in three Japanese greenlings (Hexagrammidae). Ichthyol Res 47:287–292

    Article  Google Scholar 

  • Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719

    PubMed  Google Scholar 

  • Oshima Y, Nakamura C (1942) Life history of Hexagrammos otakii (in Japanese). Suisangaku kaihou 9:81–89

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Ross CL, Harrison RG (2002) A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution 56:2296–2312

    PubMed  Google Scholar 

  • Ross CL, Benedix JH, Garcia C, Lambeth K, Perry R, Selwyn V, Howard DJ (2008) Scale-independent criteria and scale-dependent agents determining the structure of a ground cricket mosaic hybrid zone (Allonemobius sociusAllonemobius fasciatus). Biol J Linn Soc Lond 94:777–796

    Article  Google Scholar 

  • Rutenberg EP (1970) Survey of the fishes of family Hexagrammidae. In: Rass TS (ed) Greenlings: taxonomy, biology and interoceanic transplantation. Israel Program for Scientific Translations, Moskva, pp 1–103

    Google Scholar 

  • Schlefer EK, Romano MA, Guttman SI, Rush SB (1986) Effects of twenty years of hybridization in a disturbed habitat on Hyla cinerea and Hyla gratiosa. J Herpetol 20:210–221

    Article  Google Scholar 

  • Scribner KT, Page KS, Bartron ML (2001) Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev Fish Biol Fish 10:293–323

    Article  Google Scholar 

  • Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44

    Article  PubMed  Google Scholar 

  • Takahashi A, Tsaur SC, Coyne JA, Wu CI (2001) The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc Natl Acad Sci USA 98:3920–3925

    Article  CAS  PubMed  Google Scholar 

  • Takayama T (2004) Breakwater. In: Japanese Association for Coastal Zone Studies (ed) Encyclopedia of coastal zone environment (in Japanese). Kyoritsu Shuppan, Tokyo, pp 83–84

  • Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Article  Google Scholar 

  • Yamamoto G, Nishioka C (1948) Breeding habits and developmental process of greenling; Hexagrammos otakii Jordan & Starks (in Japanese with English abstract). Seibutu 3:167–170

    Google Scholar 

  • Yanchukov A, Hofman S, Szymura JM, Mezhzherin SV (2006) Hybridization of Bombina bombina and B-variegata (Anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution 60:583–600

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Masakado Kawata, John Bower, Satoshi Awata, Yoko Iwata, Karen Crow, and Ayumi Tezuka for reading this manuscript and providing valuable comments, Drs. H. Yasui, H. Mizuta and T. Kawagoe for advice on the classification of seaweeds, and Dr. S. Mawatari for identification of bryozoans. This work was supported by a grant in aid for scientific research from the Ministry of Education.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Motoko R. Kimura.

Appendix

Appendix

See Tables 4 and 5.

Table 4 Sessile organisms collected in territory sampling
Table 5 Sessile organisms collected in area sampling

About this article

Cite this article

Kimura, M.R., Munehara, H. The disruption of habitat isolation among three Hexagrammos species by artificial habitat alterations that create mosaic-habitat. Ecol Res 25, 41–50 (2010). https://doi.org/10.1007/s11284-009-0624-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-009-0624-3

Keywords

Navigation